"Although worker honey bees cannot mate, they do possess ovaries and can produce viable eggs; hence they do have the potential to have male offspring (in bees and other Hymenoptera, fertilized eggs produce females while unfertilized eggs produce males). It is now clear, however, that this potential is exceedingly rarely realized as long as a colony contains a queen (in queenless colonies, workers eventually lay large numbers of male eggs; see the review in Page and Erickson 1988). One supporting piece of evidence comes from studies of worker ovary development in queenright colonies, which have consistently revealed extremely low levels of development. All studies to date report far fewer than 1 % of workers have ovaries developed sufficiently to lay eggs (reviewed in Ratnieks 1993; see also Visscher 1995a). For example, Ratnieks dissected 10,634 worker bees from 21 colonies and found that only 7 had moderately developed egg (half the size of a completed egg) and that just one had a fully developed egg in her body."

A particular source of variation in male mating success is male size. Honey bee males are normally reared in special “drone” cells, which are larger (∼6.2 mm diameter) than the cells used for rearing workers (5.2–5.8 mm diameter) (Winston 1995). However, males can also be reared in worker cells. These resulting males are smaller in body size than normal-sized males, with fewer spermatozoa (though proportionally more relative to body size; Schluns et al. 2003), but are otherwise identical and have the same access to nutrition as adults. These “small” males may make up as much as 9% of the males in a drone congregation area (Berg 1991) and are successful at mating and fathering offspring (Berg et al. 1997; Schluns et al. 2003). Precisely how successful they are though is unknown, and quantifying this will reveal the extent of sexual selection on male size.

In addition, the relative success of small males has important implications for understanding the reproductive behavior of honey bee workers. Most males are reared from unfertilized queen-laid eggs (Ratnieks and Keller 1998), but a small proportion of workers lay unfertilized (male) eggs, even in a colony with a queen (Page and Erickson 1988; Ratnieks 1993). Intriguingly, they do this preferentially in drone cells (Page and Erickson 1988; Ratnieks 1993), even though worker cells are far more numerous. We hypothesize that this preference may be due to kin selection. Individual workers have an incentive to lay eggs because a worker is more related to sons (0.5) than brothers (queen’s sons, 0.25) (Ratnieks 1988). However, queenright honey bee colonies regulate the total number of males reared, so if workers’ sons are reared, this will reduce the number of queen’s sons. If the success of small males per unit investment is less than half that of normal-sized males, then a worker will achieve greater inclusive fitness by helping rear an additional normal-sized brother rather than a small male that is her own son. That is, egg-laying workers may only be able to enhance their inclusive fitness if they lay their eggs in drone cells. Thus, the effect of male size on mating success (sexual selection) may have an important effect on reducing intracolony conflict over male production (kin selection) (Boomsma 2007).

We found clear evidence that small honey bee males were less successful at mating than normal-sized males. Small males, introduced at a frequency similar to that under natural conditions (Berg 1991), obtained approximately half the number of matings expected, given both the numbers of males marked and the numbers observed flying. In addition, small males that did mate obtained only 61% of the paternity share obtained by normal-sized males, very close to what is expected given that they have only 63% of the spermatozoa of a normal-sized male (Schluns et al. 2003). In some other insects, small males can be more successful at mating in swarms due to their greater agility (Neems et al. 1992), but this therefore does not appear to be the case in honey bees. Small males were also observed to fly at a more constant rate in the afternoon observation period than normal males, who had a distinct peak in flight activity. The lower mating success of small males could therefore be because they flew at times of day when fewer queens were available or because they are less successful in male–male competition. The latter seems more likely. The large size of normal males is presumably under strong selective pressure because it affords greater mating success, and it seems probable that small males may be weaker fliers or less able to detect queens (Thornhill and Alcock 1983). Perhaps, therefore, the observed tendency of small males to fly earlier and later in the day may be an adaptation to exploit times when normal-sized male activity is lower and competition less. Intriguingly, all 3 of the queens that mated with small males did so twice. Possibly, these queens selected their mates differently to other queens, but more probably they flew earlier or later in the day, when relatively more small males were in the mating area. This conforms to our anecdotal observations: Although the majority of queens confined their mating flights to a narrow time window, a few queens flew earlier and later in the afternoon. Such a change in small male behavior to exploit times of day with lower competition would mirror the pattern previously noted across the mating season (Berg et al. 1997), and seen in other animals (Alcock 2005).

In terms of inclusive fitness, workers could benefit from laying eggs in worker cells if the fitness of their resulting male offspring per unit of investment is at least half (a proportion determined by the relative amount of shared genes between sons vs. brothers) that of their brothers reared in drone cells. Our results, however, suggest that the fitness of small males is less than this. Small males obtained approximately half the number of matings of normal-sized males, and those small males that did mate also obtained only 61% of the paternity of normal-sized males, which matches well with data showing that they have only 63% as many spermatozoa (Schluns et al. 2003). Small males were 70% as big as normal-sized males, so their relative fitness per unit of investment was 43% of normal-sized males, below the 50% threshold at which a worker benefits more from the colony investing in a normal-sized brother than a small son. The relatively low fitness of small males helps explain why workers, when they lay eggs, do so specifically in drone cells rather than in the more numerous workers cells (Ratnieks 1993). By reducing the opportunities for personal reproduction to enhance inclusive fitness, sexual selection on male size therefore further biases the inclusive fitness dynamics within honey bee colonies toward worker cooperation.